Chronic inhibition of cyclic guanosine monophosphate-specific phosphodiesterase 5 prevented cardiac fibrosis through inhibition of transforming growth factor β-induced Smad signaling

Frontiers of Medicine

Volumn 8, Issue 4, 2014, Pages 445-455

  Gong, Wei ^a   Yan, Mengwen ^a   Chen, Junxiong ^a   Chaugai, Sandip ^a   Chen, Chen ^a   Wang, Daowen ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

cardiac fibrosis; CREB; PDE5; TGF

Indexed keywords

GUANOSINE PHOSPHATE; MADH2 PROTEIN, RAT; MADH3 PROTEIN, RAT; PHOSPHODIESTERASE V; PHOSPHODIESTERASE V INHIBITOR; PIPERAZINE DERIVATIVE; PURINE DERIVATIVE; SILDENAFIL; SMAD PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SULFONAMIDE; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL; C57BL MOUSE; CELL CULTURE; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBROBLAST; FIBROSIS; HEART; MALE; MOUSE; RAT; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 5; ENZYME-LINKED IMMUNOSORBENT ASSAY; FIBROBLASTS; FIBROSIS; GUANOSINE MONOPHOSPHATE; HEART; MALE; MICE; MICE, INBRED C57BL; PHOSPHODIESTERASE 5 INHIBITORS; PIPERAZINES; PURINES; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SMAD PROTEINS; SMAD2 PROTEIN; SMAD3 PROTEIN; SULFONAMIDES; TRANSFORMING GROWTH FACTOR BETA;

EID: 84943406729     PISSN: 20950217     EISSN: 20950225     Source Type: Journal    
DOI: 10.1007/s11684-014-0378-3     Document Type: Article

References (37)

1. Mudd JO, Kass DA. Tackling heart failure in the twenty-first century. Nature 2008; 451(7181): 919–928
2. Berk BC, Fujiwara K, Lehoux S. ECM remodeling in hypertensive heart disease. J Clin Invest 2007; 117(3): 568–575
3. Chen J, Shearer GC, Chen Q, Healy CL, Beyer AJ, Nareddy VB, Gerdes AM, Harris WS, O’Connell TD, Wang D. Omega-3 fatty acids prevent pressure overload-induced cardiac fibrosis through activation of cyclic GMP/protein kinase G signaling in cardiac fibroblasts. Circulation 2011; 123(6): 584–593
4. Leask A. TGFbeta, cardiac fibroblasts, and the fibrotic response. Cardiovasc Res 2007; 74(2): 207–212
5. Kai H, Kuwahara F, Tokuda K, Imaizumi T. Diastolic dysfunction in hypertensive hearts: roles of perivascular inflammation and reactive myocardial fibrosis. Hypertens Res 2005; 28(6): 483–490
6. Kuwahara F, Kai H, Tokuda K, Kai M, Takeshita A, Egashira K, Imaizumi T. Transforming growth factor-beta function blocking prevents myocardial fibrosis and diastolic dysfunction in pressure-overloaded rats. Circulation 2002; 106(1): 130–135
7. Li P, Wang D, Lucas J, Oparil S, Xing D, Cao X, Novak L, Renfrow MB, Chen YF. Atrial natriuretic peptide inhibits transforming growth factor beta-induced Smad signaling and myofibroblast transformation in mouse cardiac fibroblasts. Circ Res 2008; 102(2): 185–192
8. Shi X, Yang X, Chen D, Chang Z, Cao X. Smad1 interacts with homeobox DNA-binding proteins in bone morphogenetic protein signaling. J Biol Chem 1999; 274(19): 13711–13717
9. Kass DA, Champion HC, Beavo JA. Phosphodiesterase type 5: expanding roles in cardiovascular regulation. Circ Res 2007; 101(11): 1084–1095
10. Omori K, Kotera J. Overview of PDEs and their regulation. Circ Res 2007; 100(3): 309–327
11. Takimoto E, Champion HC, Li M, Belardi D, Ren S, Rodriguez ER, Bedja D, Gabrielson KL, Wang Y, Kass DA. Chronic inhibition of cyclic GMP phosphodiesterase 5A prevents and reverses cardiac hypertrophy. Nat Med 2005; 11(2): 214–222
12. Hassan MA, Ketat AF. Sildenafil citrate increases myocardial cGMP content in rat heart, decreases its hypertrophic response to isoproterenol and decreases myocardial leak of creatine kinase and troponin T. BMC Pharmacol 2005; 5(1): 10
13. + exchanger blockade and protection against myocardial infarction. Hypertension 2007; 49(5): 1095–1103
14. Nagendran J, Archer SL, Soliman D, Gurtu V, Moudgil R, Haromy A, St Aubin C, Webster L, Rebeyka IM, Ross DB, Light PE, Dyck JR, Michelakis ED. Phosphodiesterase type 5 is highly expressed in the hypertrophied human right ventricle, and acute inhibition of phosphodiesterase type 5 improves contractility. Circulation 2007; 116(3): 238–248
15. Pokreisz P, Vandenwijngaert S, Bito V, Van den Bergh A, Lenaerts I, Busch C, Marsboom G, Gheysens O, Vermeersch P, Biesmans L, Liu X, Gillijns H, Pellens M, Van Lommel A, Buys E, Schoonjans L, Vanhaecke J, Verbeken E, Sipido K, Herijgers P, Bloch KD, Janssens SP. Ventricular phosphodiesterase-5 expression is increased in patients with advanced heart failure and contributes to adverse ventricular remodeling after myocardial infarction in mice. Circulation 2009; 119(3): 408–416
16. deAlmeida AC, van Oort RJ, Wehrens XH. Transverse aortic constriction in mice. J Vis Exp 2010; (38): e1729
17. Ni L, Zhou C, Duan Q, Lv J, Fu X, Xia Y, Wang DW. β-AR blockers suppresses ER stress in cardiac hypertrophy and heart failure. PLoS ONE 2011; 6(11): e27294
18. Villarreal FJ, Kim NN, Ungab GD, Printz MP, Dillmann WH. Identification of functional angiotensin II receptors on rat cardiac fibroblasts. Circulation 1993; 88(6): 2849–2861
19. Wang H, Lin L, Jiang J, Wang Y, Lu ZY, Bradbury JA, Lih FB, Wang DW, Zeldin DC. Up-regulation of endothelial nitric-oxide synthase by endothelium-derived hyperpolarizing factor involves mitogen-activated protein kinase and protein kinase C signaling pathways. J Pharmacol Exp Ther 2003; 307(2): 753–764
20. Soeki T, Kishimoto I, Okumura H, Tokudome T, Horio T, Mori K, Kangawa K. C-type natriuretic peptide, a novel antifibrotic and antihypertrophic agent, prevents cardiac remodeling after myocardial infarction. J Am Coll Cardiol 2005; 45(4): 608–616
21. Hammermeister KE, DeRouen TA, Dodge HT. Variables predictive of survival in patients with coronary disease. Selection by univariate and multivariate analyses from the clinical, electrocardiographic, exercise, arteriographic, and quantitative angiographic evaluations. Circulation 1979; 59(3): 421–430
22. Annes JP, Munger JS, Rifkin DB. Making sense of latent TGFbeta activation. J Cell Sci 2003; 116(2): 217–224
23. Ruiz-Ortega M, Rodríguez-Vita J, Sanchez-Lopez E, Carvajal G, Egido J. TGF-beta signaling in vascular fibrosis. Cardiovasc Res 2007; 74(2): 196–206
24. Isono M, Chen S, Hong SW, Iglesias-de la Cruz MC, Ziyadeh FN. Smad pathway is activated in the diabetic mouse kidney and Smad3 mediates TGF-beta-induced fibronectin in mesangial cells. Biochem Biophys Res Commun 2002; 296(5): 1356–1365
25. Dennler S, Itoh S, Vivien D, ten Dijke P, Huet S, Gauthier JM. Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitortype 1 gene. EMBO J 1998; 17(11): 3091–3100
26. Chen SJ, Yuan W, Lo S, Trojanowska M, Varga J. Interaction of smad3 with a proximal smad-binding element of the human alpha2 (I) procollagen gene promoter required for transcriptional activation by TGF-beta. J Cell Physiol 2000; 183(3): 381–392
27. Yang YC, Piek E, Zavadil J, Liang D, Xie D, Heyer J, Pavlidis P, Kucherlapati R, Roberts AB, Böttinger EP. Hierarchical model of gene regulation by transforming growth factor beta. Proc Natl Acad Sci USA 2003; 100(18): 10269–10274
28. Massagué J, Seoane J, Wotton D. Smad transcription factors. Genes Dev 2005; 19(23): 2783–2810
29. Buxton IL, Duan D. Cyclic GMP/protein kinase G phosphorylation of Smad3 blocks transforming growth factor-beta-induced nuclear Smad translocation: a key antifibrogenic mechanism of atrial natriuretic peptide. Circ Res 2008; 102(2): 151–153
30. Lu Z, Xu X, Hu X, Lee S, Traverse JH, Zhu G, Fassett J, Tao Y, Zhang P, dos Remedios C, Pritzker M, Hall JL, Garry DJ, Chen Y. Oxidative stress regulates left ventricular PDE5 expression in the failing heart. Circulation 2010; 121(13): 1474–1483
31. Nagayama T, Hsu S, Zhang M, Koitabashi N, Bedja D, Gabrielson KL, Takimoto E, Kass DA. Sildenafil stops progressive chamber, cellular, and molecular remodeling and improves calcium handling and function in hearts with pre-existing advanced hypertrophy caused by pressure overload. J Am Coll Cardiol 2009; 53(2): 207–215
32. Hsu S, Nagayama T, Koitabashi N, Zhang M, Zhou L, Bedja D, Gabrielson KL, Molkentin JD, Kass DA, Takimoto E. Phosphodiesterase 5 inhibition blocks pressure overload-induced cardiac hypertrophy independent of the calcineurin pathway. Cardiovasc Res 2009; 81(2): 301–309
33. Schiller M, Verrecchia F, Mauviel A. Cyclic adenosine 3′,5′-monophosphate-elevating agents inhibit transforming growth factor-beta-induced SMAD3/4-dependent transcription via a protein kinase A-dependent mechanism. Oncogene 2003; 22(55): 8881–8890
34. Gonzalez GA, Montminy MR. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 1989; 59(4): 675–680
35. Gonzalez GA, Yamamoto KK, Fischer WH, Karr D, Menzel P, Biggs W 3rd, Vale WW, Montminy MR. A cluster of phosphorylation sites on the cyclic AMP-regulated nuclear factor CREB predicted by its sequence. Nature 1989; 337(6209): 749–752
36. Liu X, Sun SQ, Hassid A, Ostrom RS. cAMP inhibits transforming growth factor-beta-stimulated collagen synthesis via inhibition of extracellular signal-regulated kinase 1/2 and Smad signaling in cardiac fibroblasts. Mol Pharmacol 2006; 70(6): 1992–2003
37. Zhang X, Yan G, Ji J, Wu J, Sun X, Shen J, Jiang H, Wang H. PDE5 inhibitor promotes melanin synthesis through the PKG pathway in B16 melanoma cells. J Cell Biochem 2012; 113(8): 2738–2743